Article Behavioral Responses of Thrips hawaiiensis (Thysanoptera: Thripidae) to Volatile Compounds Identified from Gardenia jasminoides Ellis (Gentianales: Rubiaceae)
Yu Cao 1 , Jie Wang 1, Giacinto Salvatore Germinara 2, Lijuan Wang 1, Hong Yang 1, Yulin Gao 3,* and Can Li 1,* 1 Guizhou Provincial Key Laboratory for Rare Animal and Economic Insect of the Mountainous Region, Department of Biology and Engineering of Environment, Guiyang University, Guiyang 550005, China; [email protected] (Y.C.); [email protected] (J.W.); [email protected] (L.W.); [email protected] (H.Y.) 2 Department of the Sciences of Agriculture, Food and Environment, University of Foggia, 71122 Foggia, Italy; [email protected] 3 Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China * Correspondence: [email protected] (Y.G.); [email protected] (C.L.); Tel.: +86-13552643313 (Y.G.); +86-13511965681 (C.L.); Fax: +86-10-62815930 (Y.G.); +86-851-85405891 (C.L.) Received: 16 May 2020; Accepted: 25 June 2020; Published: 1 July 2020
Abstract: Thrips hawaiiensis is a common thrips pest of various plant flowers with host preference. Plant volatiles provide important information for host-searching in insects. We examined the behavioral responses of T. hawaiiensis adults to the floral volatiles of Gardenia jasminoides Ellis, Gerbera jamesonii Bolus, Paeonia lactiflora Pallas, and Rosa chinensis Jacq. in a Y-tube olfactometer. T. hawaiiensis adults showed significantly different preferences to these four-flower plants, with the ranking of G. jasminoides > G. jamesonii > P. lactiflora R. chinensis. Further, 29 components were identified ≥ in the volatile profiles of G. jasminoides, and (Z)-3-hexenyl tiglate (14.38 %), linalool (27.45 %), and(E3,E7)-4,8,12-trimethyltrideca-1,3,7,11-tetraene(24.67%)werethemostabundant. Six-armolfactometer bioassays showed that T. hawaiiensis had significant positive responses to (Z)-3-hexenyl tiglate, linalool, and (E3,E7)-4,8,12-trimethyltrideca-1,3,7,11-tetraene tested at various concentrations, with the most 3 2 attractive ones being 10− µL/µL, 10− µL/µL and 100 µg/µL for each compound, respectively. In pairing of these three compounds at their optimal concentrations, T. hawaiiensis showed the preference ranking of (Z)-3-hexenyl tiglate > linalool > (E3,E7)-4,8,12-trimethyltrideca-1,3,7,11-tetraene. Large numbers of T. hawaiiensis have been observed on G. jasminoides flowers in the field, which might be caused by the high attraction of this pest to G. jasminoides floral volatiles shown in the present study. Our findings shed light on the olfactory cues routing host plant searching behavior in T. hawaiiensis, providing important information on how T. hawaiiensis targets particular host plants. The high attractiveness of the main compounds (e.g., linalool, (E3,E7)-4,8,12-trimethyltrideca-1,3,7,11-tetraene, particular (Z)-3-hexenyl tiglate) identified from volatiles of G. jasminoides flowers may be exploited further to develop novel monitoring and control tools (e.g., lure and kill strategies) against this flower-inhabiting thrips pest.
Keywords: olfactory responses; flower host plant; VOC; Y-tube olfactometer; six-arm olfactometer
1. Introduction Thrips hawaiiensis Morgan (Thysanoptera: Thripidae) is a common flower-dwelling thrips pest of various horticultural plant species [1,2]. Native to the Oriental and Pacific regions, T. hawaiiensis
Insects 2020, 11, 408; doi:10.3390/insects11070408 www.mdpi.com/journal/insects Insects 2020, 11, 408 2 of 11 is nowadays distributed in Asia, America, Africa, Australia, and Europe due to the expansion of international trade in fresh flowers, fruits, and vegetables [3–6]. In the field, T. hawaiiensis can attack a large number of plant species such as banana, mango, citrus, apple, tobacco, coffee, tea, horticultural plants and vegetables [6–8]. Therefore, it has become an important agricultural pest globally. Chemical insecticides have always been the primary tool for T. hawaiiensis control, especially the high number of specific treatments applied on banana and mango crops [9–11]. T. hawaiiensis showed the potential to rapidly develop resistance to insecticides (e.g., spinetoram) under laboratory selection [9,10]. Early detection of thrips is important for growers to decide when best to apply chemical insecticides or when to alter them, which would help to limit the frequency of insecticide applications, delaying the development of insecticide-resistance. Understanding the host-location behavior in thrips would be helpful for the development of monitoring tools for their early detection. The color, shape and volatiles associated with different plant species were considered to provide vital cues for thrips and help them to search and locate more suitable host plants [12–16]. Many studies have evaluated the olfactory responses of thrips, e.g., the western flower thrips Frankliniella occidentalis Pergande (Thysanoptera: Thripidae), indicating that both floral volatiles and non-floral odors were attractive to this pest [14,16–18]. Further, it was reported that rose volatile compounds allowed the design of new control strategies for western flower thrips [19]. So far little information has been mentioned on the behavioral responses of T. hawaiiensis to plant volatiles. As a polyphagous flower-inhabiting thrips in China, T. hawaiiensis is always the dominant thrips pest on many banana and mango orchards during their flowering stages [9–11,20]. In addition, T. hawaiiensis varies in its population size on different flower host plants and vegetable crops at the flowering stage and particularly showed a preference for Gardenia jasminoides Ellis (Gentianales: Rubiaceae) flowers [21,22]. These results indicated that host plant flowers had a great attractiveness to T. hawaiiensis. To contribute to the knowledge on the role of volatile compounds in the host-searching behavior of T. hawaiiensis, the olfactory responses of adult insects to the odors of different flower plants including G. jasminoides, Gerbera jamesonii Bolus (Campanulales: Asteraceae), Paeonia lactiflora Pallas (Ranales: Ranunculaceae), and Rosa chinensis Jacq. (Rosales: Rosaceae) and to the main components identified from the preferred flower plant (G. jasminoides) were studied. These results may also help in developing new monitoring tools and other control options, which could be implemented in integrated pest management (IPM) strategies against T. hawaiiensis.
2. Materials and Methods
2.1. Insects and Plants Mixed populations of T. hawaiiensis collected from various host plant species in the Nanming District, Guiyang area (26◦340 N, 106◦420 E) of Guizhou Province, China were used to establish a laboratory colony [21]. The independent colony was continuously reared for more than three generations on bean pods, Phaseolus vulgaris L. (Fabales: Leguminosae) in plastic containers [21,23]. The containers were kept in a climate-controlled room at 26 1 C, 65 5% RH and a 14:10 h ± ◦ ± light:dark photoperiod. G. jasminoides, G. jamesonii, P. lactiflora, and R. chinensis were grown in greenhouses in the nursery of Guiyang University, Guizhou Province, China. The greenhouses were maintained pest free by covering vent openings with insect-proof nettings. No pesticides were used in the whole plant growing season. Flowers at anthesis with intact petals were collected for olfactory tests and analysis of volatiles.
2.2. Behavioural Responses of T. hawaiiensis to Flower Volatiles The olfactory responses of T. hawaiiensis were tested in a Y-tube olfactometer using the method described in Cao et al. [15,23]. Two types of two-way comparisons were made: (1) each plant flower versus clean air (CA); and (2) all possible flowers pairing. The flow rate was 300 mL/min. All bioassays were conducted between 8:00 a.m. and 6:00 p.m. in a room under 26 1 C, 65 5% RH, and 1000 lux ± ◦ ± Insects 2020, 11, 408 3 of 11 illumination conditions. For each comparison, 50 females that were 2–3 days old were tested. Thrips were starved for 4 h before the bioassay and the flower material (15.0 g) was replaced after every 10 tested individuals.
2.3. Collection and Analysis of Volatile Organic Compounds (VOCs) Flower volatiles were collected and analyzed as described in Cao et al. [16]. Flower material (0.3 g) excised from a given host plant was kept in a glass bottle (200 mL) for 2 h prior to capturing the volatiles emitted using a solid-phase microextraction fiber (a ~50/30 µm DVB/CAR/PDMS StableFlex fiber). Volatiles were extracted for 40 min at 80 ◦C then the fiber head was quickly removed. The collected volatiles were analyzed by gas chromatography mass spectrometry (GC–MS) (HP6890/5975C, Agilent Technologies, CA, USA). The chromatographic column was a ZB-5MSI 5% phenyl-95% dimethylpolysiloxane elastic quartz capillary vessel column (30 m 0.25 mm 0.25 µm). × × The gas chromatograph was operated at an initial temperature of 40 ◦C for 2 min then increased at 5 ◦C/min to 255 ◦C, which was maintained for 2 min. To identify compounds, we compared the mass spectra of compounds with those in databases (Nist 2005 and Wiley 275) and their constituents were confirmed through coinjections with authentic standards.
2.4. Behavioural Responses of T. hawaiiensis to the Main G. jasminoides Volatile Organic Compounds (VOCs) The VOC mixture from G. jasminoides was the most attractive to T. hawaiiensis as assessed by the Y-tube olfactometer bioassays. Since linalool, (Z)-3-hexenyl tiglate and (E3,E7)-4,8,12-trimethyltrideca-1,3,7,11- tetraene were the most abundant compounds identified in the VOC profile of G. jasminoides, the behavioral responses of T. hawaiiensis to these compounds were tested further in six-arm and Y-tube olfactometer bioassays.
2.5. Odour Stimuli Mineral oil (Sigma-Aldrich, Steinheim, Germany) solutions of linalool and (Z)-3-hexenyl tiglate 5 4 3 2 1 (Sigma-Aldrich, Germany; chemical purity 99%) (i.e., 10− , 10− , 10− , 10− and 10− µL/µL) and (E3,E7)-4,8,12-trimethyltrideca-1,3,7,11-tetraene (Sigma-Aldrich, Germany; chemical purity 99%) (i.e., 0.1, 1, 10, 100 and 200 µg/µL) were prepared. Solutions were stored at 20 C until the testing phase. − ◦ 2.6. Six-arm Olfactometer Bioassays The behavioral responses of adult T. hawaiiensis to different doses of linalool, (Z)-3-hexenyl tiglate, and (E3,E7)-4,8,12-trimethyltrideca-1,3,7,11-tetraene) were evaluated in a six-arm olfactometer with the method described by Liu et al. [24]. and Cao et al. [25]. Briefly, the six-arm olfactometer consisted of a central chamber with six arms, each connected to a glass tube that projected outwards at an equidistance, with equal angles (60◦) between pairs of tubes. Each arm was connected through Teflon tubing to a glass vessel containing a test or control stimulus. For each experiment, equal volumes (25 µL) of each of the five solutions of one compound and mineral oil (used as the control), absorbed onto a filter paper disk (1.0-cm diameter), were used as test and control stimuli, respectively. The airflow was set at 200 mL/min to drive the odor source to thrips. Thrips hawaiiensis (2–3 days old females) were starved for 4 h and introduced in groups (200 individuals per group) into the central chamber with a fine camel hair brush. Within 20 min, insects that entered one arm of the olfactometer were counted as having made a choice for a particular odor, while thrips that did not enter any arm were considered non-responders. After each test, the olfactometer was cleaned, dried and the arms were rotated (60◦). Each bioassay was replicated six times between 9:00 am and 6:00 pm. In order to eliminate any light bias, a 25-W light was placed in the center 60 cm above the chamber. Insects 2019, 10, x 4 of 11 times between 9:00 am and 6:00 pm. In order to eliminate any light bias, a 25-W light was placed in the center 60 cm above the chamber.
2.7.Insects Y-Tube2020, 11Bioassays, 408 4 of 11 In the six-arm olfactometer bioassays, linalool, (Z)-3-hexenyl tiglate, and (E3,E7)-4,8,12-trimethyltrideca2.7. Y-Tube Bioassays -1,3,7,11-tetraene showed the highest attractiveness to T. hawaiiensis at the concentration of 10−2 μL/μL, 10−3 μL/μL and 100 μg/μL, respectively. Therefore, the attractant powerIn of thethe six-armthree compounds olfactometer at their bioassays, optimal linalool, concentrations (Z)-3-hexenyl were compared tiglate, andin further (E3,E7)-4,8,12- Y-tube bioassaystrimethyltrideca-1,3,7,11-tetraene as described above. showed the highest attractiveness to T. hawaiiensis at the concentration 2 3 of 10− µL/µL, 10− µL/µL and 100 µg/µL, respectively. Therefore, the attractant power of the three 2.8.compounds Statistical at Analyses their optimal concentrations were compared in further Y-tube bioassays as described above.
2.8.All Statistical statistical Analyses analyses were performed using SPSS 18.0 for Windows (SPSS Inc., Chicago, IL, USA) [26]. The null hypothesis that T. hawaiiensis adults showed no preference for either Y-tube arm (a responseAll statistical equal to analyses 50:50) werewas performedanalyzed using using a SPSS chi-square 18.0 for Windowsgoodness-of-fit (SPSS Inc.,test Chicago,[27]. The IL, number USA) [26of ]. thripsThe null found hypothesis in the different that T. hawaiiensis arms of adultsthe six-arm showed olfactometer no preference were for eithersubjected Y-tube to armFriedman (a response two-way equal ANOVAto 50:50) by was ranks analyzed and in using the case a chi-square of significance goodness-of-fit (p < 0.05) test the [ 27Wilcoxon]. The number signed ofranks thrips test found was used in the fordifferent separation arms of of means the six-arm [28]. olfactometer were subjected to Friedman two-way ANOVA by ranks and in the case of significance (p < 0.05) the Wilcoxon signed ranks test was used for separation of means [28]. 3. Results 3. Results
3.1.3.1. Behavioural Behavioural Responses Responses of of T. T. hawaiiensis hawaiiensis to to Flower Flower Volatiles Volatiles WhenWhen T.T. hawaiiensis hawaiiensis adults were presentedpresented with with di differentfferent flower flower volatiles volatilesversus versusclean clean air (CA),air (CA), they 2 2 theyshowed showed significant significant preferences preferences for G. for jasminoides G. jasminoides(χ2 = (25.13,߯ = 25.13,df = 1,dfp =< 1,0.01), p < 0.01),G. jamesonii G. jamesonii(χ2 = (16.20,߯ = ߯2 ߯2 16.20,df = 1,dfp =< 1,0.01), p < 0.01),P. lactiflora P. lactiflora(χ2 = 5.82,( = df5.82,= 1, dfp == 1,0.016) p = 0.016) and R. and chinensis R. chinensis(χ2 = 5.00,( = df5.00,= 1, dfp == 1,0.025) p = 0.025)(Figure (Figure1). 1).
FigureFigure 1. 1. BehavioralBehavioral responses responses of of T.T. hawaiiensis hawaiiensis toto the the volatiles volatiles from from diffe differentrent flowers. flowers. Asterisks Asterisks indicateindicate highly highly significant significant (** (** p p< <0.01)0.01) and and significant significant (* p (*
>0.05)0.05) in in the the selectivityselectivity of of T.T. hawaiiensis hawaiiensis betweenbetween two two odors. odors.
ThripsThrips hawaiiensis hawaiiensis alsoalso showed showed significant significant preferences preferences among among the the flowers flowers when when presented presented with with 2 choices.choices. GardeniaGardenia jasminoides jasminoides waswas more more attractive attractive to to T.T. hawaiiensis hawaiiensis thanthan G.G. jamesonii jamesonii (߯(2χ = 4.79,= 4.79, df df= 1,= p1, p = 0.029), P. lactiflora (χ2 = 6.15, df = 1, p = 0.013) or R. chinensis (χ2 = 8.02, df = 1, p = 0.005). Gardenia jasminoides was more attractive than P. lactiflora (χ2 = 4.26, df = 1, p = 0.039) or R. chinensis (χ2 = 5.23, df = 1, p = 0.022). However, T. hawaiiensis showed no significant preference between P. lactiflora and R. chinensis (χ2 = 2.69, df = 1, p = 0.10) (Figure1). Insects 2020, 11, 408 5 of 11
3.2. Analysis of G. jasminoides Volatiles Twenty-nine components were identified in the volatiles from G. jasminoides (Table1). The component with the highest relative content was linalool (27.45%), followed by (E3,E7)-4,8,12-trimethyltrideca-1,3,7,11-tetraene (24.67%), (Z)-3-hexenyl tiglate (14.38%), and then jasmine lactone (6.93%). There was no other component greater than 5% identified from the flower volatiles of G. jasminoides.
Table 1. Volatile components of G. jasminoides flower.
Number Compounds Molecular Formula Molecular Weight Content (%)
1 Methyl tiglate C6H10O2 114 0.39 2 (Z)-3-Hexen-1-ol C6H12O 100 3.59 3 β-Myrcene C10H16 136 0.15 4 (Z)-3-Hexenyl acetate C8H14O2 142 0.18 5 (E)-Ocimene C10H16 136 1.38 6 γ-Caprolactone C6H10O2 114 0.10 7 trans-Linalool oxide C10H18O2 170 0.32 8 Methyl benzoate C8H8O2 136 1.64 9 Linalool C10H18O 154 27.45 10 (Z)-3-hexenyl iso-butyrate C10H18O2 134 0.22 11 Benzyl acetate C9H10O2 150 0.25 12 (Z)-3-hexenyl butanoate C10H18O2 170 0.38 13 Methyl salicylate C8H8O3 152 0.20 14 (Z)-3-hexenyl 2-methylbutanoate C11H20O2 184 1.28 15 Hexyl 2-Methylbutyrate C11H22O2 186 0.61 16 Benzyl propionate C10H12O2 164 0.12 17 (Z)-3-hexenyl tiglate C11H18O2 182 14.38 18 Hexyl tiglate C11H20O2 184 4.01 19 (Z)-3-hexenyl hexanoate C12H22O2 198 0.11 20 Isoamyl benzoate C12H16O2 192 0.28 21 γ-Decanolactone C10H18O2 170 0.18 22 Jasmine lactone C10H16O2 168 6.93 23 Benzyl tiglate C12H14O2 190 0.23 24 α-Farnesene C15H24 204 3.58 25 Octyl (E)-2-methylbut-2-enoate C13H24O2 212 0.58 26 E-Nerolidol C15H26O 222 0.27 27 (Z)-3-Hexenyl phenylacetate C14H18O2 218 0.41 28 (E3,E7)-4,8,12-trimethyltrideca-1,3,7,11-tetraene C16H26 218 24.67 29 Geranyl tiglate C15H24O2 236 0.41
3.3. Behavioural Responses of T. hawaiiensis to the Main Components of G. jasminoides VOCs
3.3.1. Six-Arm Olfactometer Bioassays In these experiments, the number of insects that entered the control arm connected to the vessel with mineral oil were significantly lower than those of insects found in the arms with the different doses of linalool (Friedman test: χ2 = 30.00, df = 5, p < 0.001, Wilcoxon tests: p = 0.026–0.028), (Z)-3-hexenyl tiglate (Friedman test: χ2 = 29.88, df = 5, p < 0.001, Wilcoxon tests: p = 0.026–0.027), or (E3,E7)-4,8,12-trimethyltrideca-1,3,7,11-tetraene (Friedman test: χ2 = 29.88, df = 5, p < 0.001, Wilcoxon tests: p = 0.026–0.028) (Figure2). Insects 2020, 11, 408 6 of 11 Insects 2019, 10, x 6 of 11
100 f 80
60 e 40 d Thrips (n.) Thrips c b 20 a 0 2.5 0.25 0.025 0.0025 0.00025 Control Linalool (µl ) 100
80 f e 60
40 d Thrips (n.) b c 20 a 0 2.5 0.25 0.025 0.0025 0.00025 Control (Z)-3-hexenyl tiglate (µl) 100
80 f e 60
40 d Thrips (n.) c b 20 a 0 5 2.5 0.25 0.025 0.0025 Control (E3,E7)-4,8,12-trimethyltrideca-1,3,7,11-tetraene (mg)
Figure 2. Olfactory responses of T. hawaiiensis to different doses of linalool, (Z)-3-hexenyl tiglate and (E3,E7)-4,8,12-trimethyltrideca-1,3,7,11-tetraeneFigure 2. Olfactory responses of T. hawaiiensis in to a different six-arm olfactometer.doses of linaloo Controll, (Z)-3-hexenyl was mineral tiglate oil. and Each box(E3,E7)-4,8,12-trimethyltrideca-1,3,7,11-tetraene plot represents the median and its range of dispersion in a six-arm (lower olfactometer. and upper quartiles Control and was outliers). mineral oil. AboveEach each box plot,plot represents different letters the median indicate and significant its rang dieff oferences dispersion (Wilcoxon (lower test, andp < upper0.05). quartiles and outliers). Above each box plot, different letters indicate significant differences (Wilcoxon test, p < There0.05). were relatively significant differences in attraction among all doses of linalool (Wilcoxon tests: p = 0.026–0.028), (Z)-3-hexenyl tiglate (Wilcoxon tests: p = 0.026–0.038), and (E3,E7)-4,8,12- There were relatively significant differences in attraction among all doses of linalool (Wilcoxon tests: p = 0.026–0.028), (Z)-3-hexenyl tiglate (Wilcoxon tests: p = 0.026–0.038), and
Insects 2020, 11, 408 7 of 11 Insects 2019, 10, x 7 of 11
2 trimethyltrideca-1,3,7,11-tetraene(E3,E7)-4,8,12-trimethyltrideca-1,3,7,11-tetraene (Friedman test: χ =(Friedman29.88, df = test:5, p <χ20.001, = 29.88, Wilcoxon df = 5, tests:p < 0.001,p = 0.026–0.043) Wilcoxon (Figuretests: p3 =). 0.026–0.043) Significantly (Figure more insects 3). Significantly entered the more arm connectedinsects entered to the the vessel arm that connected contained to 0.25the vesselµL of linaloolthat contained or 0.025 µ L0.25 of (Z)-3-hexenyl μL of linalool tiglate oror 0.25 0.025 mg ofμ (E3,E7)-4,8,12-trimethyltrideca-1,3,7,11-tetraeneL of (Z)-3-hexenyl tiglate or 0.25 mg over of the(E3,E7)-4,8,12-trimethyltrideca arm with the other doses. -1,3,7,11-tetraene over the arm with the other doses.
Figure 3. Behavioral responses of T. hawaiiensis to the main Ga. jasminoides volatiles. Asterisks Figure 3. Behavioral responses of T. hawaiiensis to the main Ga. jasminoides volatiles. Asterisks indicate indicate highly significant (** p < 0.01) and significant (* p < 0.05) differences in the selectivity of T. highly significant (** p < 0.01) and significant (* p < 0.05) differences in the selectivity of T. hawaiiensis hawaiiensis between two odors by ߯2 test. between two odors by χ2 test.
3.3.2.3.3.2. Y-Tube OlfactometerOlfactometer BioassaysBioassays
2 -2 3 -3 InIn thethe six-arm six-arm olfactometer olfactometer bioassays, bioassays, 10− 10µL/μµLL/ forμL linalool,for linalool, 10− µ10L/µ Lμ forL/μ (Z)-3-hexenylL for (Z)-3-hexenyl tiglate andtiglate 100 andµg/µ L100 for μ (E3,E7)-4,8,12-trimethyltrideca-1,3,7,11-tetraene,g/μL for (E3,E7)-4,8,12-trimethyltrideca-1,3,7,11-tetraene, respectively, wererespectively, the most attractivewere the concentrationsmost attractive to concentrationsT. hawaiiensis .to Thus, T. hawaiiensis the behavioral. Thus, responses the behavioral of T. hawaiiensis responsesto of these T. hawaiiensis compounds to atthese their compounds optimal doses at their were optimal further doses compared were in furthe a Y-tuber compared olfactometer in a Y-tube (Figure olfactometer3). Significantly (Figure higher 3). numbersSignificantly of T. higher hawaiiensis numberswere of foundT. hawaiiensis to prefer were (Z)-3-hexenyl found to prefer tiglate (Z)-3-hexenyl (χ2 = 27.00, tiglatedf = 1, (χp2 <= 27.00,0.01), linalooldf = (χ1,2 = 25.13,p
Insects 2020, 11, 408 8 of 11
GC-MS analysis highlighted the presence of 29 compounds in the VOC profile of G. jasminoides flowers, among which the most abundant compounds, linalool (27.45 %), (E3,E7)-4,8,12-trimethyltrideca-1,3,7,11- tetraene (24.67 %), and (Z)-3-hexenyl tiglate (14.38 %), were considered to be related to the typical floral 5 1 odor of this plant species [36]. Different concentrations of linalool (10− ~ 10− µL/µL), (Z)-3-hexenyl 5 1 tiglate (10− ~ 10− µL/µL), and (E3,E7)-4,8,12-trimethyltrideca-1,3,7,11-tetraene (0.1 ~ 200 µg/µL) were all 2 3 attractive to T. hawaiiensis, but the 10− µL/µL, 10− µL/µL, and 100 µg/µL concentrations, respectively, were the most attractive ones. Further, regarding these three compounds at their optimal attractive concentration, T. hawaiiensis had different olfactory preferences with (Z)-3-hexenyl tiglate > linalool > (E3,E7)-4,8,12-trimethyltrideca-1,3,7,11-tetraene. Therefore, (Z)-3-hexenyl tiglate seems to have greater potential for the development of a new attractant lure for T. hawaiiensis monitoring and control. The behavioral responses of insects are influenced not only by individual compounds and concentrations but also by their ratios in mixtures [37–39]. So, the possible additive or synergistic effects among (Z)-3-hexenyl tiglate and the other attractive compounds identified in this study may require to be further evaluated through massive behavioral bioassays testing different doses and combinations of these VOCs. Moreover, field-trapping tests should be conducted to confirm their practically attractive effects [18,19,30,37]. Pollens were considered to be an important factor involved in the preference of thrips for host plant flowers [40–42], as F. occidentalis was attracted to the compound of (S)-verbenone identified from the volatiles of pine pollen [18,33]. However, pollens of G. jasminoides flowers were not involved in T. hawaiiensis’ olfactory responses in this study. Besides, the host preference of different thrips species were related to the color, shape, nutritional conditions or other physicochemical characteristics of host plants [13,15,17,43–45]. Thus, more related physicochemical characteristics that may influence the behavioral responses of T. hawaiiensis should be studied to comprehensively understand the mechanism of host selection among different flower plants. Host plant volatiles not only attract phytophagous pests but also their natural enemies [46–48] Although predators seem to be more attracted by herbivore-induced volatiles, as reported on the significant preferences of the predator Neoseiulus cucumeris Oudemans (Acari: Phytoseiidae) to the volatiles from vegetable hosts infested by F. occidentalis or Thrips tabaci Lindeman (Lindeman) (Thysanoptera: Thripidae) [47,49], data that do not support such a specificity have been reported [50–53]. In this framework, it is imperative to study the attractiveness of VOCs from healthy and infested flowers to natural enemies of T. hawaiiensis, e.g., Orius sauteri Poppius (Heteroptera: Anthocoridae) [54].
5. Conclusions Females of T. hawaiiensis exhibited a higher olfactory preference for the VOCs of G. jasminoides flowers over a range of four flower plants. Moreover, insects were significantly attracted by different concentrations of the three main components of G. jasminoides flower VOCs with (Z)-3-hexenyl tiglate being the most attractive. Overall, this study clearly demonstrated that plant volatiles are involved in host-plant selection by T. hawaiiensis even if, to comprehensively understand this mechanism, possible interactions among chemical cues and other physicochemical characteristics remain to be investigated. The kairomonal activity of (Z)-3-hexenyl tiglate, linalool, and (E3,E7)-4,8,12-trimethyltrideca-1,3,7,11-tetraene to T. hawaiiensis females found in this study provides a basis for further electrophysiological, behavioral, and field-trapping experiments to develop semiochemically-based monitoring tools and direct control options for this pest.
Author Contributions: Y.C., Y.G. and C.L. conceived and designed the research. J.W., L.W. and H.Y. conducted the experiments. Y.C. and G.S.G. analyzed the data. Y.C. and G.S.G. wrote the manuscript. All authors have read and agreed to the published version of the manuscript. Funding: This research was funded by the Provincial Natural Science Foundation of Guizhou, grant number [2018]1004; the Regional First-class Discipline Construction of Guizhou Province, grant number [2017]85; Discipline and Master’s Site Construction Project of Guiyang University financed by Guiyang City, grant number SH-2020; the Program for Academician Workstation in Guiyang University, grant number 20195605; and the Training Project for High-Level Innovative Talents in Guizhou Province, grant number 2016 [4020] and The APC was funded by Guizhou Provincial Key Laboratory for Rare Animal and Economic Insect of the Mountainous Region. Conflicts of Interest: The authors declare no conflict of interest. Insects 2020, 11, 408 9 of 11
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